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Intensity-dependent host mortality: what can it tell us about larval growth strategies in complex life cycle helminths?

Published online by Cambridge University Press:  18 April 2011

Department of Evolutionary Ecology, Max-Planck-Institute for Evolutionary Biology, August-Thienemann-Strasse 2, 24306 Plön, Germany
*Corresponding author: Tel: +49 4522 763262. Fax: +49 4522 763310. E-mail:


Complex life cycle helminths use their intermediate hosts as both a source of nutrients and as transportation. There is an assumed trade-off between these functions in that parasite growth may reduce host survival and thus transmission. The virulence of larval helminths can be assessed by experimentally increasing infection intensities and recording how parasite biomass and host mortality scale with intensity. I summarize the literature on these relationships in larval helminths and I provide an empirical example using the nematode Camallanus lacustris in its copepod first host. In all species studied thus far, including C. lacustris, overall parasite volume increases with intensity. Although a few studies observed host survival to decrease predictably with intensity, several studies found no intensity-dependent mortality or elevated mortality only at extreme intensities. For instance, no intensity-dependent mortality was observed in male copepods infected with C. lacustris, whereas female survival was reduced only at high intensities (>3) and only after worms were fully developed. These observations suggest that at low, natural intensity levels parasites do not exploit intermediate hosts as much as they presumably could and that increased growth would not obviously entail survival costs.

Research Article
Copyright © Cambridge University Press 2011

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Abrams, P. A., Leimar, O., Nylin, S. and Wiklund, C. (1996). The effect of flexible growth rates on optimal sizes and development times in a seasonal environment. American Naturalist 147, 381395.CrossRefGoogle Scholar
Amin, O. M., Burns, L. A. and Redlin, M. J. (1980). Ecology of Acanthocephalus parksidei Amin, 1975 (Acanthocephala, Echinorhynchidae) in its isopod intermediate host. Proceedings of the Helminthological Society of Washington 47, 3746.Google Scholar
Andersen, P. K. (1991). Survival analysis 1982–1991 - the 2nd decade of the proportional hazards regression-model. Statistics in Medicine 10, 19311941.CrossRefGoogle Scholar
Anderson, R. C. (2000). Nematode Parasites of Vertebrates: Their Development and Transmission, CABI, Wallingford, UK.CrossRefGoogle Scholar
Anderson, R. M. and May, R. M. (1978). Regulation and stability of host-parasite population interactions I. Regulatory processes. Journal of Animal Ecology 47, 219247.CrossRefGoogle Scholar
Awachie, J. B. E. (1966). The development and life-history of Echinorhynchus truttae Schrank 1788 (Acanthocephala). Journal of Helminthology 40, 1132.CrossRefGoogle ScholarPubMed
Ball, M. A., Parker, G. A. and Chubb, J. C. (2008). The evolution of complex life cycles when parasite mortality is size- or time-dependent. Journal of Theoretical Biology 253, 202214.CrossRefGoogle ScholarPubMed
Bates, A. E., Poulin, R. and Lamare, M. D. (2010). Spatial variation in parasite-induced mortality in an amphipod: shore height versus exposure history. Oecologia 163, 651659.CrossRefGoogle Scholar
Benesh, D. P. (2010 a). Developmental inflexibility of larval tapeworms in response to resource variation. International Journal for Parasitology 40, 487497.CrossRefGoogle ScholarPubMed
Benesh, D. P. (2010 b). What are the evolutionary constraints on larval growth in a trophically transmitted parasite? Oecologia 162, 599608.CrossRefGoogle Scholar
Benesh, D. P., Chubb, J. C. and Parker, G. A. (2011). Exploitation of the same trophic link favors convergence of larval life history strategies in complex life cycle helminths. Evolution (in the Press).CrossRefGoogle ScholarPubMed
Benesh, D. P. and Valtonen, E. T. (2007). Effects of Acanthocephalus lucii (Acanthocephala) on intermediate host survival and growth: implications for exploitation strategies. Journal of Parasitology 93, 735741.CrossRefGoogle ScholarPubMed
Brattey, J. (1986). Life-history and population biology of larval Acanthocephalus lucii (Acanthocephala, Echinorhynchidae) in the isopod Asellus aquaticus. Journal of Parasitology 72, 633645.CrossRefGoogle ScholarPubMed
Brown, S. P., De Lorgeril, J., Joly, C. and Thomas, F. (2003). Field evidence for density-dependent effects in the trematode Microphallus papillorobustus in its manipulated host, Gammarus insensibilis. Journal of Parasitology 89, 668672.CrossRefGoogle ScholarPubMed
Brown, S. P., Loot, G., Grenfell, B. T. and Guegan, J. F. (2001). Host manipulation by Ligula intestinalis: accident or adaptation? Parasitology 123, 519529.CrossRefGoogle ScholarPubMed
Calentine, R. L. (1965). Biology and taxonomy of Biacetabulum (Cestoda: Caryophyllaeidae). Journal of Parasitology 51, 243248.CrossRefGoogle Scholar
Cawthorn, R. J. and Anderson, R. C. (1976). Effects of age, temperature, and previous infection on the development of Physaloptera maxillaris (Nematoda: Physalopteroidea) in field crickets (Acheta pennsylvanicus). Canadian Journal of Zoology 54, 442448.CrossRefGoogle ScholarPubMed
Choisy, M., Brown, S. P., Lafferty, K. D. and Thomas, F. (2003). Evolution of trophic transmission in parasites: why add intermediate hosts? American Naturalist 162, 172181.CrossRefGoogle ScholarPubMed
Chubb, J. C., Ball, M. A. and Parker, G. A. (2010). Living in intermediate hosts: evolutionary adaptations in larval helminths. Trends in Parasitology 26, 93102.CrossRefGoogle ScholarPubMed
Cornet, S. (2011). Density-dependent effects on parasite growth and parasite-induced host immunodepression in the larval helminth Pomphorhynchus laevis. Parasitology 138, 257265.CrossRefGoogle ScholarPubMed
Courtney, C. C. and Christensen, B. M. (1987). Host-parasite relationships of caryophyllaeid cestodes and aquatic oligochaetes I. Host longevity and parasite intensity. Journal of Parasitology 73, 11241132.CrossRefGoogle Scholar
Crofton, H. D. (1971). Quantitative approach to parasitism. Parasitology 62, 179193.CrossRefGoogle Scholar
Day, T. (2003). Virulence evolution and the timing of disease life-history events. Trends in Ecology and Evolution 18, 113118.CrossRefGoogle Scholar
Day, T. and Rowe, L. (2002). Developmental thresholds and the evolution of reaction norms for age and size at life-history transitions. American Naturalist 159, 338350.CrossRefGoogle ScholarPubMed
Denny, M. (1969). Life-cycles of helminth parasites using Gammarus lacustris as an intermediate host in a Canadian lake. Parasitology 59, 795827.CrossRefGoogle Scholar
Dezfuli, B. S., Giari, L. and Poulin, R. (2001). Costs of intraspecific and interspecific host sharing in acanthocephalan cystacanths. Parasitology 122, 483489.CrossRefGoogle ScholarPubMed
Duclos, L. M., Danner, B. J. and Nickol, B. B. (2006). Virulence of Corynosoma constrictum (Acanthocephala: Polymorphidae) in Hyalella azteca (Amphipoda) throughout parasite ontogeny. Journal of Parasitology 92, 749755.CrossRefGoogle ScholarPubMed
Ferreira, S. M., Jensen, K. T., Martins, P., Sousa, S. F., Marques, J. C. and Pardal, M. A. (2005). Impact of microphallid trematodes on the survivorship, growth, and reproduction of an isopod (Cyathura carinata). Journal of Experimental Marine Biology and Ecology 318, 191199.CrossRefGoogle Scholar
Fredensborg, B. L., Mouritsen, K. N. and Poulin, R. (2004). Intensity-dependent mortality of Paracalliope novizealandiae (Amphipoda: Crustacea) infected by a trematode: experimental infections and field observations. Journal of Experimental Marine Biology and Ecology 311, 253265.CrossRefGoogle Scholar
Fredensborg, B. L. and Poulin, R. (2005). Larval helminths in intermediate hosts: does competition early in life determine the fitness of adult parasites? International Journal for Parasitology 35, 10611070.CrossRefGoogle ScholarPubMed
Freeman, R. S. (1952). Temperature as a factor affecting development of Monoecocestus (Cestoda: Anoplocephalidae) in oribatid mites. Experimental Parasitology 1, 256262.CrossRefGoogle Scholar
Gandon, S. (2004). Evolution of multihost parasites. Evolution 58, 455469.Google ScholarPubMed
Gotthard, K. (2001). Growth strategies of ectothermic animals in temperate environments. In Environment and Animal Development (ed. Thorndyke, D. A. M.), pp. 287304. BIOS Scientific Publishers, Oxford , UK.Google Scholar
Guinnee, M. A. and Moore, J. (2004). The effect of parasitism on host fecundity is dependent on temperature in a cockroach-acanthocephalan system. Journal of Parasitology 90, 673677.CrossRefGoogle Scholar
Hansen, E. K. and Poulin, R. (2005). Impact of a microphallid trematode on the behaviour and survival of its isopod intermediate host: phylogenetic inheritance? Parasitology Research 97, 242246.CrossRefGoogle ScholarPubMed
Heins, D. C., Baker, J. A. and Martin, H. C. (2002). The “crowding effect” in the cestode Schistocephalus solidus: density-dependent effects on plerocercoid size and infectivity. Journal of Parasitology 88, 302307.Google Scholar
Heins, D. C., Birden, E. L. and Baker, J. A. (2010). Host mortality and variability in epizootics of Schistocephalus solidus infecting the threespine stickleback, Gasterosteus aculeatus. Parasitology 137, 16811686.CrossRefGoogle ScholarPubMed
Huizinga, H. W. (1967). The life cycle of Contracaecum multipapillatum (Von Drasche, 1882) Lucker, 1941 (Nematoda: Heterochelidae). The Journal of Parasitology 53, 368375.CrossRefGoogle ScholarPubMed
Hurd, H., Warr, E. and Polwart, A. (2001). A parasite that increases host lifespan. Proceedings of the Royal Society of London, B 268, 17491753.CrossRefGoogle ScholarPubMed
Iwasa, Y. and Wada, G. (2006). Complex life cycle and body sizes at life-history transitions for macroparasites. Evolutionary Ecology Research 8, 14271443.Google Scholar
Keymer, A. E. (1980). The influence of Hymenolepis diminuta on the survival and fecundity of the intermediate host, Tribolium confusum. Parasitology 81, 405421.CrossRefGoogle ScholarPubMed
Kisielewska, K. (1959). Types of Copepoda and Drepanidotaenia lanceolata (Bloch) host-parasite systems established experimentally. Acta Parasitologica Polonica 7, 371392.Google Scholar
Kokkotis, T. and McLaughlin, J. D. (2006). Pathogenicity of the hymenolepidid cestode Microsomacanthus hopkinsi in its intermediate host, Hyalella azteca: implications for transmission, host fitness, and host populations. Canadian Journal of Zoology 84, 3241.CrossRefGoogle Scholar
Korting, W. (1975). Larval development of Bothriocephalus sp (Cestoda: Pseudophyllidea) from carp (Cyprinus carpio L.) in Germany. Journal of Fish Biology 7, 727733.CrossRefGoogle Scholar
Lagrue, C. and Poulin, R. (2008). Intra-and interspecific competition among helminth parasites: effects on Coitocaecum parvum life history strategy, size and fecundity. International Journal for Parasitology 38, 14351444.CrossRefGoogle ScholarPubMed
Latham, A. D. M. and Poulin, R. (2002). Field evidence of the impact of two acanthocephalan parasites on the mortality of three species of New Zealand shore crabs (Brachyura). Marine Biology 141, 11311139.Google Scholar
Lopez, C., Panadero, R., Diez, P. and Morrondo, P. (1998). Effect of the infection by Neostrongylus linearis on the survival of the intermediate host Cernuella (cernuella) virgata. Parasite 5, 181184.CrossRefGoogle ScholarPubMed
Measures, L. N. (1988). The development of Eustrongylides tubifex (Nematoda, Dioctophymatoidea) in oligochaetes. Journal of Parasitology 74, 294304.CrossRefGoogle ScholarPubMed
Meissner, K. and Bick, A. (1999). Mortality of Corophium volutator (Amphipoda) caused by infestation with Maritrema subdolum (Digenea, Microphallidae) - laboratory studies. Diseases of Aquatic Organisms 35, 4752.CrossRefGoogle Scholar
Metcalfe, N. B. and Monaghan, P. (2001). Compensation for a bad start: grow now, pay later? Trends in Ecology and Evolution 16, 254260.CrossRefGoogle ScholarPubMed
Michaud, M., Milinski, M., Parker, G. A. and Chubb, J. C. (2006). Competitive growth strategies in intermediate hosts: experimental tests of a parasite life-history model using the cestode, Schistocephalus solidus. Evolutionary Ecology 20, 3957.CrossRefGoogle Scholar
Moravec, F. (1978). The development of the nematode Philometra obturans (Prenant, 1886) in the intermediate host. Folia Parasitologica 25, 303315.Google Scholar
Moravec, F. (1969). Observations on the development of Camallanus lacustris (Zoega, 1776). Vèstnik Ceskoslovenské Zoologické Spolecnosti 33, 1533.Google Scholar
Nie, P. and Kennedy, C. R. (1993). Infection dynamics of larval Bothriocephalus claviceps in Cyclops vicinus. Parasitology 106, 503509.CrossRefGoogle Scholar
Okaka, C. E. (1989). Studies on the development of the oncosphere and procercoid of Cyathocephalus truncatus (Cestoda) in the intermediate host, Gammarus pulex. Zoologica Scripta 18, 205209.CrossRefGoogle Scholar
Outreman, Y., Cezilly, F. and Bollache, L. (2007). Field evidence of host size-dependent parasitism in two manipulative parasites. Journal of Parasitology 93, 750754.CrossRefGoogle ScholarPubMed
Parker, G. A., Ball, M. A. and Chubb, J. C. (2009 a). To grow or not to grow? Intermediate and paratenic hosts as helminth life cycle strategies. Journal of Theoretical Biology 258, 135147.CrossRefGoogle ScholarPubMed
Parker, G. A., Ball, M. A. and Chubb, J. C. (2009 b). Why do larval helminths avoid the gut of intermediate hosts? Journal of Theoretical Biology 260, 460473.CrossRefGoogle ScholarPubMed
Parker, G. A., Chubb, J. C., Ball, M. A. and Roberts, G. N. (2003 a). Evolution of complex life cycles in helminth parasites. Nature, London 425, 480484.CrossRefGoogle ScholarPubMed
Parker, G. A., Chubb, J. C., Roberts, G. N., Michaud, M. and Milinski, M. (2003 b). Optimal growth strategies of larval helminths in their intermediate hosts. Journal of Evolutionary Biology 16, 4754.CrossRefGoogle ScholarPubMed
Pilecka-Rapacz, M. (1986). On the development of acanthocephalans of the genus Acanthocephalus Koelreuther, 1771, with special attention to their influence on intermediate host, Asellus aquaticus L. Acta Parasitologica Polonica 30, 233250.Google Scholar
Ponton, F., Lalubin, F., Fromont, C., Wilson, K., Behm, C. and Simpson, S. J. (2011). Hosts use altered macronutrient intake to circumvent parasite-induced reduction in fecundity. International Journal for Parasitology 41, 4350.CrossRefGoogle ScholarPubMed
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Poulin, R., Curtis, M. A. and Rau, M. E. (1992). Effects of Eubothrium salvelini (Cestoda) on the behavior of Cyclops vernalis (Copepoda) and its susceptibility to fish predators. Parasitology 105, 265271.CrossRefGoogle Scholar
Poulin, R. and Latham, A. D. M. (2003). Effects of initial (larval) size and host body temperature on growth in trematodes. Canadian Journal of Zoology 81, 574581.CrossRefGoogle Scholar
Poulin, R., Nichol, K. and Latham, A. D. A. (2003). Host sharing and host manipulation by larval helminths in shore crabs: cooperation or conflict? International Journal for Parasitology 33, 425433.CrossRefGoogle ScholarPubMed
Robert, F. and Gabrion, C. (1991). Experimental approach to the specificity in first intermediate hosts of Bothriocephalids (Cestoda, Pseudophyllidea) from marine fish. Acta Oecologica 12, 617632.Google Scholar
Rosen, L., Ash, L. R. and Wallace, G. D. (1970). Life history of canine lungworm Angiostrongylus vasorum (Baillet). American Journal of Veterinary Research 31, 131139.Google ScholarPubMed
Rosen, R. and Dick, T. A. (1983). Development and infectivity of the procercoid of Triaenophorus crassus Forel and mortality of the first intermediate host. Canadian Journal of Zoology 61, 21202128.CrossRefGoogle Scholar
Sakanari, J. and Moser, M. (1985). Salinity and temperature effects on the eggs, coracidia, and procercoids of Lacistorhynchus tenuis (Cestoda, Trypanorhyncha) and induced mortality in a first intermediate host. Journal of Parasitology 71, 583587.CrossRefGoogle Scholar
Saldanha, I., Leung, T. L. F. and Poulin, R. (2009). Causes of intraspecific variation in body size among trematode metacercariae. Journal of Helminthology 83, 289293.CrossRefGoogle ScholarPubMed
Sandland, G. J. and Goater, C. P. (2000). Development and intensity dependence of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows (Pimephales promelas). Journal of Parasitology 86, 10561060.CrossRefGoogle ScholarPubMed
Shostak, A. W., Rosen, R. B. and Dick, T. A. (1985). The use of growth-curves to assess the crowding effect on procercoids of the tapeworm Triaenophorus crassus in the copepod host Cyclops bicuspidatus thomasi. Canadian Journal of Zoology 63, 23432351.CrossRefGoogle Scholar
Shostak, A. W., Walsh, J. G. and Wong, Y. C. (2008). Manipulation of host food availability and use of multiple exposures to assess the crowding effect on Hymenolepis diminuta in Tribolium confusum. Parasitology 135, 10191033.CrossRefGoogle ScholarPubMed
Skorping, A. (1984). Density-dependent effects in a parasitic nematode, Elaphostrongylus rangiferi, in the snail intermediate host. Oecologia 64, 3440.CrossRefGoogle Scholar
Skorping, A. (1985). Parasite-induced reduction in host survival and fecundity - the effect of the nematode Elaphostrongylus rangiferi on the snail intermediate host. Parasitology 91, 555562.CrossRefGoogle Scholar
Solomon, A., Paperna, I. and Alkon, P. U. (1996). The suitability of Trochoidea seetzenii of different ages as snail intermediate hosts of Muellerius cf. capillaris (Nematoda: Protostrongylidae). International Journal for Parasitology 26, 13171319.CrossRefGoogle ScholarPubMed
Steinauer, M. L. and Nickol, B. B. (2003). Effect of cystacanth body size on adult success. Journal of Parasitology 89, 251254.CrossRefGoogle ScholarPubMed
Thomas, F., Renaud, F., Rousset, F., Cezilly, F. and Demeeus, T. (1995). Differential mortality of two closely-related host species induced by one parasite. Proceedings of the Royal Society of London, B 260, 349352.Google Scholar
Trowe, S. (1997). Morphometrical differentiation of Anoplocephalidae cysticeroids with a contribution to reproduction of oribatid mites experimentally infected. Ph.D. thesis, Freie Universität Berlin, Germany.Google Scholar
Uznanski, R. L. and Nickol, B. B. (1980). Parasite population regulation: lethal and sublethal effects of Leptorhynchoides thecatus (Acanthocephala, Rhadinorhynchidae) on Hyalella azteca (Amphipoda). Journal of Parasitology 66, 121126.CrossRefGoogle Scholar
Valkounova, J. (1980). The most important factors affecting the larval development of cestodes of the family Hymenolepididae in crustaceans (Copepoda). Vèstnik Ceskoslovenské Zoologické Spolecnosti 44, 230240.Google Scholar
Van der Veen, I. T. and Kurtz, J. (2002). To avoid or eliminate: cestode infections in copepods. Parasitology 124, 465474.CrossRefGoogle ScholarPubMed
Werner, E. E. and Gilliam, J. F. (1984). The ontogenetic niche and species interactions in size structured populations. Annual Review of Ecology and Systematics 15, 393425.CrossRefGoogle Scholar
Wootten, R. (1974). Studies on the life history and development of Proteocephalus percae (Müller) (Cestoda: Proteocephalidea). Journal of Helminthology 48, 269281.CrossRefGoogle ScholarPubMed